The IL-1β/STAT1 Axis inhibits STAT3 function via Sequestration of the transcriptional activator GLIS2, leading to postoperative vascular dysfunction

Int Immunopharmacol. 2024 Dec 25;143(Pt 2):113372. doi: 10.1016/j.intimp.2024.113372. Epub 2024 Oct 17.

Abstract

Surgery-induced endothelial dysfunction is crucial in thrombus formation, driven by the release of inflammatory mediators due to surgical trauma. The STAT family, known for amplifying inflammatory responses via cytokine activation, plays an unclear role in the signaling mechanisms from surgery to molecular activation, and their regulatory effects on inflammation vary. This study aimed to identify key signaling pathways responsible for vascular dysfunction post-surgery and to discover potential targets for predicting or preventing thrombosis. To explore this, endothelial cells were co-cultured with post-surgical trauma serum and analyzed using various assays. Bioinformatics analysis linked surgical trauma with pathways involving thrombosis, interleukins, cytokines, and STAT signaling. Elevated inflammatory mediators were observed in mouse serum post-surgical trauma, with IL-6 activating STAT3 to enhance endothelial proliferation, while IL-1β activated STAT1, inhibiting STAT3's effects. Gli-similar 2 (GLIS2), a novel coactivator of STAT3, was found to regulate STAT transcription. STAT1, however, inhibited GLIS2's interaction with STAT3, suppressing STAT3's role in endothelial proliferation. The study concludes that IL-1β-triggered STAT1 activation impedes GLIS2-STAT3 interaction, reducing STAT3's transcriptional activity and leading to endothelial dysfunction, presenting new targets for preventing post-surgical trauma endothelial dysfunction and thrombosis.

Keywords: Endothelial dysfunction; GLIS2; STAT; Surgical trauma; Transcriptional co-factor.

MeSH terms

  • Animals
  • Cell Proliferation
  • Endothelial Cells / metabolism
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Interleukin-1beta* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Postoperative Complications / metabolism
  • STAT1 Transcription Factor* / metabolism
  • STAT3 Transcription Factor* / metabolism
  • Signal Transduction*
  • Thrombosis / metabolism

Substances

  • STAT1 Transcription Factor
  • STAT3 Transcription Factor
  • Interleukin-1beta
  • Stat1 protein, mouse